Lower dietary n-6 : n-3 ratio and high-dose vitamin E supplementation improve sperm morphology and oxidative stress in boars
Qing Liu A , Yuanfei Zhou A , Runjia Duan A , Hongkui Wei A , Siwen Jiang B C D and Jian Peng A C D
+ Author Affiliations
- Author Affiliations
A Department of Animal Nutrition and Feed Science, College of Animal Science and Technology, Huazhong Agricultural University, 430070, Wuhan, P. R. China.
B Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education and Key Lab of Swine Genetics and Breeding of Ministry of Agriculture, Huazhong Agricultural University, 430070, Wuhan, P. R. China.
C The Cooperative Innovation Center for Sustainable Pig Production, Wuhan 430070, P. R. China.
D Corresponding authors. Emails: pengjian@mail.hzau.edu.cn; jiangsiwen@mail.hzau.edu.cn
Reproduction, Fertility and Development 29(5) 940-949 https://doi.org/10.1071/RD15424
Submitted: 15 October 2015 Accepted: 14 January 2016 Published: 9 March 2016
Abstract
A 2 × 2 factorial experiment (10 boars per treatment) was conducted for 16 weeks to evaluate the effects of the dietary n-6 : n-3 ratio (14 : 1 vs 6 : 1) and vitamin E (200 vs 400 mg kg–1) on boar sperm morphology and oxidative stress. Sperm mitochondrial membrane potential (MMP), reactive oxygen species (ROS), DNA damage (8-hydroxydeoxyguanosine; 8-OHdG), seminal lipoperoxidation (malondialdehyde; MDA) and antioxidant capacity in the serum, spermatozoa and seminal plasma were assessed as indicators of oxidative stress. Sperm production was similar among groups but increased (P < 0.05) throughout the 16 weeks of the study. Although sperm α-tocopherol content, ROS and seminal MDA did not differ between the two dietary n-6 : n-3 ratio treatments, enhanced antioxidant enzyme activity and MMP, but decreased 8-OHdG, were found in spermatozoa from boars consuming the 6 : 1 diet. The diet with the 6 : 1 ratio positively affected sperm morphology at Weeks 12 and 16 (P < 0.05). The α-tocopherol content and antioxidant capacity increased in boars with increasing levels of vitamin E supplementation. Compared with low-dose vitamin E, high-dose vitamin E supplementation improved sperm morphology. Overall, the results indicate that an n-6 : n-3 ratio of 6 : 1 and 400 mg/kg vitamin E have beneficial effects on sperm morphology by improving antioxidative stress.
Additional keywords: antioxidative effect.
References
Agarwal, A., Makker, K., and Sharma, R. (2008). Review article: clinical relevance of oxidative stress in male factor infertility: an update. Am. J. Reprod. Immunol. 59, 2–11.| Review article: clinical relevance of oxidative stress in male factor infertility: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1Wjsbc%3D&md5=e771320694b20762c1a9a27bf7b628f3CAS | 18154591PubMed |
Aldemir, M., Okulu, E., Kösemehmetoğlu, K., Ener, K., Topal, F., Evirgen, O., Gürleyik, E., and Avcı, A. (2014). Evaluation of the protective effect of quercetin against cisplatin-induced renal and testis tissue damage and sperm parameters in rats. Andrologia 46, 1089–1097.
| Evaluation of the protective effect of quercetin against cisplatin-induced renal and testis tissue damage and sperm parameters in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFShsL7K&md5=ddaf11130b5b02d7702e1c0dd6d49a4fCAS | 24266675PubMed |
Alm, K., Peltoniemi, O., Koskinen, E., and Andersson, M. (2006). Porcine field fertility with two different insemination doses and the effect of sperm morphology. Reprod. Domest. Anim. 41, 210–213.
| Porcine field fertility with two different insemination doses and the effect of sperm morphology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283ms1Wmsw%3D%3D&md5=88b0de0ec24e72ff157ca1d2d040fc71CAS | 16689883PubMed |
Audet, I., Berube, N., Bailey, J. L., Laforest, J. P., and Matte, J. J. (2009). Effects of dietary vitamin supplementation and semen collection frequency on reproductive performance and semen quality in boars. J. Anim. Sci. 87, 1960–1970.
| Effects of dietary vitamin supplementation and semen collection frequency on reproductive performance and semen quality in boars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1eju78%3D&md5=6bee9dfb8c75904ce518ec737b1adc31CAS | 19286814PubMed |
Aziz, N., Saleh, R. A., Sharma, R. K., Lewis-Jones, I., Esfandiari, N., Thomas, A. J., and Agarwal, A. (2004). Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil. Steril. 81, 349–354.
| Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFKqurk%3D&md5=4829ccb0f4a3faede070f9cace0f260eCAS | 14967372PubMed |
Brezezińska-Slebodzińska, E., Ślebodziński, A., Pietras, B., and Wieczorek, G. (1995). Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma. Biol. Trace Elem. Res. 47, 69–74.
| Antioxidant effect of vitamin E and glutathione on lipid peroxidation in boar semen plasma.Crossref | GoogleScholarGoogle Scholar | 7779577PubMed |
Chen, H., Zhao, H. X., Huang, X. F., Chen, G. W., Yang, Z. X., Sun, W. J., Tao, M. H., Yuan, Y., Wu, J. Q., and Sun, F. (2012). Does high load of oxidants in human semen contribute to male factor infertility? Antioxid. Redox Signal. 16, 754–759.
| Does high load of oxidants in human semen contribute to male factor infertility?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVyhsrk%3D&md5=cdc59955d15ab22f82ab4a3126a58330CAS | 22149455PubMed |
Comhaire, F. H., Christophe, A. B., Zalata, A. A., Dhooge, W. S., Mahmoud, A. M. A., and Depuydt, C. E. (2000). The effects of combined conventional treatment, oral antioxidants and essential fatty acids on sperm biology in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids 63, 159–165.
| The effects of combined conventional treatment, oral antioxidants and essential fatty acids on sperm biology in subfertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslGisbc%3D&md5=e7da4466bf64d707f1d625c2e7927988CAS | 10991774PubMed |
da Rocha, A. A., da Cunha, I. C. N., Ederli, B. B., Albernaz, A. P., and Quirino, C. R. (2009). Effect of daily food supplementation with essential fatty acids on canine semen quality. Reprod. Domest. Anim. 44, 313–315.
| Effect of daily food supplementation with essential fatty acids on canine semen quality.Crossref | GoogleScholarGoogle Scholar | 19754593PubMed |
De Iuliis, G. N., Thomson, L. K., Mitchell, L. A., Finnie, J. M., Koppers, A. J., Hedges, A., Nixon, B., and Aitken, R. J. (2009). DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine, a marker of oxidative stress. Biol. Reprod. 81, 517–524.
| DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine, a marker of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVChu7%2FE&md5=10a8e46dedb293938ef134691cdd7f5cCAS | 19494251PubMed |
Esmaeili, V., Shahverdi, A., Moghadasian, M., and Alizadeh, A. (2015). Dietary fatty acids affect semen quality: a review. Andrology 3, 450–461.
| Dietary fatty acids affect semen quality: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpt1WqtLs%3D&md5=097cb178d3f241312b51b7aa5c94151aCAS | 25951427PubMed |
França, L. R., Avelar, G. F., and Almeida, F. F. (2005). Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63, 300–318.
| Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs.Crossref | GoogleScholarGoogle Scholar | 15626401PubMed |
Fraser, L., and Strzezek, J. (2007). Is there a relationship between the chromatin status and DNA fragmentation of boar spermatozoa following freezing–thawing? Theriogenology 68, 248–257.
| Is there a relationship between the chromatin status and DNA fragmentation of boar spermatozoa following freezing–thawing?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFKgsLc%3D&md5=c95cc3d2bd0792eb6de5cf19d662142bCAS | 17543381PubMed |
Gong, S., Gabriel, M. C. S., Zini, A., Chan, P., and O’Flaherty, C. (2012). Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men. J. Androl. 33, 1342–1351.
| Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvFeitg%3D%3D&md5=fe792b40798933937e5f60e7fa483d6fCAS | 22492841PubMed |
Grant, S. A., Long, S. E., and Parkinson, T. J. (1994). Fertilizability and structural properties of boar spermatozoa prepared by Percoll gradient centrifugation. J. Reprod. Fertil. 100, 477–483.
| Fertilizability and structural properties of boar spermatozoa prepared by Percoll gradient centrifugation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3ptlagtw%3D%3D&md5=58021ffa70ee9e305e394a955670aadfCAS | 8021866PubMed |
Greco, E., Iacobelli, M., Rienzi, L., Ubaldi, F., Ferrero, S., and Tesarik, J. (2005). Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment. J. Androl. 26, 349–353.
| Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVWjsr8%3D&md5=3a2dfc25929ecf8ef5e45d4387b26d34CAS | 15867002PubMed |
Hancock, J., and Hovell, G. (1959). The collection of boar semen. Vet. Rec. 71, 664–665.
Kodama, H., Yamaguchi, R., Fukuda, J., Kasai, H., and Tanaka, T. (1997). Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil. Steril. 68, 519–524.
| Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svmtVGntg%3D%3D&md5=21a418331ea35f493f403444758b2b1cCAS | 9314926PubMed |
Kozink, D. M., Estienne, M. J., Harper, A. F., and Knight, J. W. (2004). Effects of dietary l-carnitine supplementation on semen characteristics in boars. Theriogenology 61, 1247–1258.
| Effects of dietary l-carnitine supplementation on semen characteristics in boars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsVOmtLc%3D&md5=b62719d9b8ae554b71e225bf7ab8162dCAS | 15036959PubMed |
Lanzafame, F. M., La Vignera, S., Vicari, E., and Calogero, A. E. (2009). Oxidative stress and medical antioxidant treatment in male infertility. Reprod. Biomed. Online 19, 638–659.
| Oxidative stress and medical antioxidant treatment in male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisVaqtg%3D%3D&md5=2dae5bc388ca11ce6019e73f8730460eCAS | 20021713PubMed |
Leahy, T., Celi, P., Bathgate, R., Evans, G., Maxwell, W., and Marti, J. (2010). Flow-sorted ram spermatozoa are highly susceptible to hydrogen peroxide damage but are protected by seminal plasma and catalase. Reprod. Fertil. Dev. 22, 1131–1140.
| Flow-sorted ram spermatozoa are highly susceptible to hydrogen peroxide damage but are protected by seminal plasma and catalase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVOgu7vI&md5=9e596909736b2d1acc00be67de8d0492CAS | 20797351PubMed |
Lenzi, A., Gandini, L., Maresca, V., Rago, R., Sgro, P., Dondero, F., and Picardo, M. (2000a). Fatty acid composition of spermatozoa and immature germ cells. Mol. Hum. Reprod. 6, 226–231.
| Fatty acid composition of spermatozoa and immature germ cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVCgurc%3D&md5=b71b0595b7ee363d12199f97236a38e0CAS | 10694269PubMed |
Lenzi, A., Gandini, L., Picardo, M., Tramer, F., Sandri, G., and Panfili, E. (2000b). Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies. Front. Biosci. 5, E1–E15.
| Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible scavenger therapies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXht1Shtbs%3D&md5=e4b88d27b5c6bf24c801aa341bb960adCAS | 10702376PubMed |
Liu, Q., Zhou, Y. F., Duan, R. J., Wei, H. K., Jiang, S. W., and Peng, J. (2015). Effects of dietary n-6 : n-3 fatty acid ratio and vitamin E on semen quality, fatty acid composition and antioxidant status in boars. Anim. Reprod. Sci. 162, 11–19.
| Effects of dietary n-6 : n-3 fatty acid ratio and vitamin E on semen quality, fatty acid composition and antioxidant status in boars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGgsLvJ&md5=b0c0ac9940af09beb38231f53890aa98CAS | 26417649PubMed |
Marin-Guzman, J., Mahan, D., Chung, Y., Pate, J., and Pope, W. (1997). Effects of dietary selenium and vitamin E on boar performance and tissue responses, semen quality, and subsequent fertilization rates in mature gilts. J. Anim. Sci. 75, 2994–3003.
| 1:CAS:528:DyaK2sXntFelsr4%3D&md5=559c3b6ba697e3689f2462670e7636a8CAS | 9374315PubMed |
Miller, N. J., Rice-Evans, C., Davies, M. J., Gopinathan, V., and Milner, A. (1993). A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Clin. Sci. 84, 407–412.
| A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3ksFCmtA%3D%3D&md5=8efaa4580b83e1ca92e47b27487a8a11CAS | 8482045PubMed |
NRC (2012) ‘Nutrient Requirements of Swine.’ 11th edn. (National Academy Press: Washington, DC.)
O’Connell, M., McClure, N., and Lewis, S. (2002). The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum. Reprod. 17, 704–709.
| The effects of cryopreservation on sperm morphology, motility and mitochondrial function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD387jsVymsQ%3D%3D&md5=6d6f02e2e6bcc6e48f87a4dc15e9e5aeCAS | 11870124PubMed |
O’Flaherty, C., and de Souza, A. R. (2011). Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol. Reprod. 84, 238–247.
| Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVelsbk%3D&md5=9629d97b112ec77a5aa551b54856042bCAS | 20864641PubMed |
Ollero, M., Gil-Guzman, E., Lopez, M. C., Sharma, R. K., Agarwal, A., Larson, K., Evenson, D., Thomas, A. J., and Alvarez, J. G. (2001). Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum. Reprod. 16, 1912–1921.
| Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntlahu78%3D&md5=9b81808b0e7b8dfdf9011c3a75ee2964CAS | 11527898PubMed |
Ombelet, W., Menkveld, R., Kruger, T., and Steeno, O. (1995). Sperm morphology assessment: historical review in relation to fertility. Hum. Reprod. Update 1, 543–557.
| Sperm morphology assessment: historical review in relation to fertility.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3jtlajtA%3D%3D&md5=b64000e129a1177a27d25cb1eded636dCAS | 9079395PubMed |
Peña, F. J., Johannisson, A., Wallgren, M., and Rodriguez Martinez, H. (2003). Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate. Anim. Reprod. Sci. 78, 85–98.
| Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate.Crossref | GoogleScholarGoogle Scholar | 12753785PubMed |
Rao, B., Soufir, J., Martin, M., and David, G. (1989). Lipid peroxidation in human spermatozoa as relatd to midpiece abnormalities and motility. Gamete Res. 24, 127–134.
| Lipid peroxidation in human spermatozoa as relatd to midpiece abnormalities and motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlvFahtL0%3D&md5=0b5bfeaea0987c57016eacd38de79ebdCAS | 2793053PubMed |
Rooke, J. A., Shao, C. C., and Speake, B. K. (2001). Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen. Reproduction 121, 315–322.
| Effects of feeding tuna oil on the lipid composition of pig spermatozoa and in vitro characteristics of semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslSisbc%3D&md5=bb9fa4d71422f6c8080f67856753dae5CAS | 11226056PubMed |
Safarinejad, M. R., Hosseini, S. Y., Dadkhah, F., and Asgari, M. A. (2010). Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin. Nutr. 29, 100–105.
| Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1antLc%3D&md5=09adeb71b8c2085bcb49d02f9e5fa5feCAS | 19666200PubMed |
Sikka, S. C. (2001). Relative impact of oxidative stress on male reproductive function. Curr. Med. Chem. 8, 851–862.
| Relative impact of oxidative stress on male reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsVChuro%3D&md5=53ebf26624f69eac0a02a08cb52fd3f3CAS | 11375755PubMed |
Strzezek, J. (2002). Secretory activity of boar seminal vesicle glands. Reprod. Biol. 2, 243–266.
| 14666148PubMed |
Strzezek, J., Fraser, L., Kuklinska, M., Dziekonska, A., and Lecewicz, M. (2004). Effects of dietary supplementation with polyunsaturated fatty acids and antioxidants on biochemical characteristics of boar semen. Reprod. Biol. 4, 271–287.
| 15592586PubMed |
Surai, P. F., Noble, R. C., Sparks, N. H., and Speake, B. K. (2000). Effect of long-term supplementation with arachidonic or docosahexaenoic acids on sperm production in the broiler chicken. J. Reprod. Fertil. 120, 257–264.
| 1:CAS:528:DC%2BD3cXovVajurw%3D&md5=e37c15f6f20e683305e8f793f1bef182CAS | 11058441PubMed |
Tremellen, K. (2008). Oxidative stress and male infertility: a clinical perspective. Hum. Reprod. Update 14, 243–258.
| Oxidative stress and male infertility: a clinical perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFOqtbc%3D&md5=0c549fa3dd4a4932c4975182d5a4f1daCAS | 18281241PubMed |
Wander, R. C., Hall, J. A., Gradin, J. L., Du, S. H., and Jewell, D. E. (1997). The ratio of dietary (n-6) to (n-3) fatty acids influences immune system function, eicosanoid metabolism, lipid peroxidation and vitamin E status in aged dogs. J. Nutr. 127, 1198–1205.
| 1:CAS:528:DyaK2sXjsFOntr4%3D&md5=72d03ab82a42351d7a00c85f142d6f47CAS | 9187636PubMed |
Wang, H., and Joseph, J. A. (1999). Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27, 612–616.
| Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls12nt7Y%3D&md5=32462c48f74e1fccd62f6d80f5f0c7fdCAS | 10490282PubMed |
Yeste, M., Barrera, X., Coll, D., and Bonet, S. (2011). The effects on boar sperm quality of dietary supplementation with omega-3 polyunsaturated fatty acids differ among porcine breeds. Theriogenology 76, 184–196.
| The effects on boar sperm quality of dietary supplementation with omega-3 polyunsaturated fatty acids differ among porcine breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFKitbc%3D&md5=9486fed191694fdd7bf50d38784fa688CAS | 21458051PubMed |
Zalata, A. A., Ahmed, A. H., Allamaneni, S., Comhaire, F. H., and Agarwal, A. (2004). Relationship between acrosin activity of human spermatozoa and oxidative stress. Asian J. Androl. 6, 313–318.
| 1:CAS:528:DC%2BD2MXjslWjsQ%3D%3D&md5=54d6f8d6bac7309789ee5d76552904ceCAS | 15546022PubMed |
Zini, A., and Libman, J. (2014) Oxidative stress and male infertility. In ‘Systems Biology of Free Radicals and Antioxidants’. (Ed. I. Laher.) pp. 2815–2833. (Springer: Berlin.)
